Arrangement of cross-bridges in insect flight muscle in rigor

Abstract

We have previously proposed that in insect flight muscle in rigor, the cross-bridges are formed by the attachment of one head of a myosin molecule to one actin filament and the other head to a neighbouring filament (Offer & Elliott, 1978). We have now analysed this type of model in more detail and considered the geometrical conditions that have to be fulfilled for such two-filament interaction to be possible. We find that two labelling patterns are possible. In both, only 2 7 of the actin subunits are labelled. In one type there is an unlabelled subunit between two labelled subunits of the long-pitched strands of the actin filament; in the other type, a similar grouping occurs in one long-pitched strand, while in the other strand there is a gap of two unlabelled subunits. We have shown that if the myosin molecules on the insect thick filament are arranged on a right-handed, four-stranded helix (Wray, 1979 a,b), it is possible to find conditions where only two-filament interaction and no single-filament interaction would be expected. In this case, approximately 9 16 of the myosin heads attach, while the remainder are unattached. With other thick filament symmetries a mixture of single-filament and two-filament interactions would be expected. The two-filament interaction type of model can, with a suitable choice of actin-myosin binding geometry, explain the appearance of transverse and longitudinal sections of insect flight muscle in rigor (Reedy, 1968). The Fourier transforms of many variations of the two-filament interaction model have been calculated. We find several detailed models, differing principally in the slew angle of attachment of myosin heads and in the position of troponin, which are able to account satisfactorily for the observed X-ray diffraction patterns of this muscle in rigor (Miller & Tregear, 1972; Holmes et al., 1980).